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Journal of Zhejiang University (Agriculture and Life Sciences)  2023, Vol. 49 Issue (6): 755-764    DOI: 10.3785/j.issn.1008-9209.2022.07.182
Reviews     
Research advances in the mechanisms of protecting animals against influenza by probiotics
Meiqing HAN1(),Di WANG1,Xianqi PENG1,Yan LI1,2()
1.Institute of Preventive Veterinary Medicine/Zhejiang Provincial Key Laboratory of Preventive Veterinary Medicine, College of Animal Sciences, Zhejiang University, Hangzhou 310058, Zhejiang, China
2.Hainan Institute of Zhejiang University, Sanya 572025, Hainan, China
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Abstract  

Influenza is an important zoonotic disease. The highly pathogenic avian influenza not only brings enormous losses to China’s livestock breeding industry but also seriously threatens the safety of public health. The ability of influenza viruses to recombine in swine and spread across species barriers poses significant challenges for influenza prevention. Due to the rapid mutation of influenza viruses, the differences between prevalent viruses and vaccine strains reduce the vaccine efficacy. It is necessary to improve the host’s immunity to influenza viruses. Probiotics regulate the balance of intestinal microbiota and promote body health, which is beneficial for protecting animal against influenza viruses. This paper reviewed the mechanisms of anti-influenza virus action of probiotics in animals. The mechanisms include direct or indirect interference with virus attacks by balancing the composition of intestinal flora, regulating the mucosal barrier function of body, and enhancing or suppressing Toll-like receptor-related molecular signaling pathways. This study provides scientific evidence for understanding the mechanisms by which different strains of probiotics combat influenza and for developing more effective anti-influenza strategies.



Key wordsinfluenza virus      probiotics      immunity      “gut-lung axis”     
Received: 18 July 2022      Published: 25 December 2023
CLC:  S85  
Corresponding Authors: Yan LI     E-mail: xxhan0818@qq.com;yanli3@zju.edu.cn
Cite this article:

Meiqing HAN,Di WANG,Xianqi PENG,Yan LI. Research advances in the mechanisms of protecting animals against influenza by probiotics. Journal of Zhejiang University (Agriculture and Life Sciences), 2023, 49(6): 755-764.

URL:

https://www.zjujournals.com/agr/10.3785/j.issn.1008-9209.2022.07.182     OR     https://www.zjujournals.com/agr/Y2023/V49/I6/755


益生菌帮助动物抵御流感的机制研究进展

流感是一种重要的人畜共患病,高致病性禽流感不仅给我国养殖业带来巨大损失,还严重威胁公共卫生安全。流感病毒能够在猪体内重组并跨越物种屏障进行传播,这给预防流感带来巨大挑战。由于流感病毒的变异速度快,流行的病毒株和疫苗株之间的差异会降低疫苗的效力,因此增强机体对流感病毒的抵抗力显得尤为重要。益生菌具有调节肠道微生物平衡、促进机体健康的作用,对动物机体抵抗流感病毒是有益的。本文综述了益生菌在动物体内抗流感病毒的作用机制,阐明了益生菌可以通过平衡动物肠道菌群组成、调节机体黏膜屏障功能、增强或抑制Toll样受体相关分子信号通路等方式直接或间接干扰病毒的侵袭,为了解不同菌种发挥抗流感的相应机制及开发更有效的抗流感策略提供了科学依据。


关键词: 流感病毒,  益生菌,  免疫,  “肠-肺轴” 
Fig. 1 Working pattern of the “gut-lung axis” during viral respiratory infectionsThis picture is created with BioRender website (https://www.biorender.com/), and the same as Fig. 2.
Fig. 2 Schematic diagram of possible effect mechanisms of probiotics against influenza virus infections
[1]   NODA T, SAGARA H, YEN A, et al. Architecture of ribonucleoprotein complexes in influenza A virus particles[J]. Nature, 2006, 439(7075): 490-492. DOI: 10.1038/nature04378
doi: 10.1038/nature04378
[2]   SHI Y, WU Y, ZHANG W, et al. Enabling the ‘host jump’: structural determinants of receptor-binding specificity in influenza A viruses[J]. Nature Reviews Microbiology, 2014, 12(12): 822-831. DOI: 10.1038/nrmicro3362
doi: 10.1038/nrmicro3362
[3]   KRAMMER F, SMITH G J D, FOUCHIER R A M, et al. Influenza[J]. Nature Reviews Disease Primers, 2018, 4: 3. DOI: 10.1038/s41572-018-0002-y
doi: 10.1038/s41572-018-0002-y
[4]   王大燕,舒跃龙.流感大流行的历史及思考[J].中国科学:生命科学,2018,48(12):1247-1251. DOI:10.1360/N052018-00205
WANG D Y, SHU Y L. History and reflection of pandemic influenza[J]. Scientia Sinica (Vitae), 2018, 48(12): 1247-1251. (in Chinese with English abstract)
doi: 10.1360/N052018-00205
[5]   杨帅,朱闻斐,舒跃龙.猪流感病毒概述[J].病毒学报,2013,29(3):330-336. DOI:10.13242/j.cnki.bingduxuebao.002395
YANG S, ZHU W F, SHU Y L. An overview on swine influenza viruses[J]. Chinese Journal of Virology, 2013, 29(3): 330-336. (in Chinese with English abstract)
doi: 10.13242/j.cnki.bingduxuebao.002395
[6]   KIM H, WEBSTER R G, WEBBY R J. Influenza virus: dealing with a drifting and shifting pathogen[J]. Viral Immunology, 2018, 31(2): 174-183. DOI: 10.1089/vim.2017.0141
doi: 10.1089/vim.2017.0141
[7]   CHANG H P, PENG L, CHEN L, et al. Avian influenza viruses (AIVs) H9N2 are in the course of reassorting into novel AIVs[J]. Journal of Zhejiang University-Science B (Biomedicine & Biotechnology), 2018, 19(5): 409-414. DOI: 10.1631/jzus.b1700374
doi: 10.1631/jzus.b1700374
[8]   SUN H L, LI F T, LIU Q Z, et al. Mink is a highly susceptible host species to circulating human and avian influenza viruses[J]. Emerging Microbes & Infections, 2021, 10(1): 472-480. DOI: 10.1080/22221751.2021.1899058
doi: 10.1080/22221751.2021.1899058
[9]   OLSEN S J, WINN A K, BUDD A P, et al. Changes in influenza and other respiratory virus activity during the COVID-19 pandemic—United States, 2020—2021[J]. American Journal of Transplantation, 2021, 21(10): 3481-3486. DOI: 10.1111/ajt.16049
doi: 10.1111/ajt.16049
[10]   WEBSTER R G, GOVORKOVA E A. Continuing challenges in influenza[J]. Annals of the New York Academy of Sciences, 2014, 1323(1): 115-139. DOI: 10.1111/nyas.12462
doi: 10.1111/nyas.12462
[11]   RODRIGUEZ L, NOGALES A, MARTÍNEZ-SOBRIDO L. Influenza A virus studies in a mouse model of infection[J]. Journal of Visualized Experiments, 2017(127): 55898. DOI: 10.3791/55898
doi: 10.3791/55898
[12]   FARRUKEE R, HURT A C. Antiviral drugs for the treatment and prevention of influenza[J]. Current Treatment Options in Infectious Diseases, 2017, 9(3): 318-332. DOI: 10.1007/s40506-017-0129-5
doi: 10.1007/s40506-017-0129-5
[13]   SÁNCHEZ B, DELGADO S, BLANCO-MÍGUEZ A, et al. Probiotics, gut microbiota, and their influence on host health and disease[J]. Molecular Nutrition & Food Research, 2017, 61(1): 1600240. DOI: 10.1002/mnfr.201600240
doi: 10.1002/mnfr.201600240
[14]   LILLY D M, STILLWELL R H. Probiotics: growth-promoting factors produced by microorganisms[J]. Science, 1965, 147(3659): 747-748.
[15]   Food and Agriculture Organization of the United Nations (FAO)/World Health Organization (WHO). Guidelines for the evaluation of probiotics in food[C]//Report of a Joint FAO/WHO Working Group on Drafting Guidelines for the Evaluation of Probiotics in Food. London, Ontario, Canada: FAO/WHO, 2002.
[16]   RUSSELL S L, GOLD M J, WILLING B P, et al. Perinatal antibiotic treatment affects murine microbiota, immune responses and allergic asthma[J]. Gut Microbes, 2013, 4(2): 158-164. DOI: 10.4161/gmic.23567
doi: 10.4161/gmic.23567
[17]   BAUD D, DIMOPOULOU AGRI V, GIBSON G R, et al. Using probiotics to flatten the curve of coronavirus disease COVID-2019 pandemic[J]. Frontiers in Public Health, 2020, 8: 186. DOI: 10.3389/fpubh.2020.00186
doi: 10.3389/fpubh.2020.00186
[18]   TAPIOVAARA L, PITKARANTA A, KORPELA R. Probiotics and upper respiratory tract—a review[J]. Pediatric Infectious Diseases Open, 2016, 1(3): 19. DOI: 10.4172/PIDO.100019
doi: 10.4172/PIDO.100019
[19]   FANOS V, PINTUS M C, PINTUS R, et al. Lung microbiota in the acute respiratory disease: from coronavirus to meta-bolomics[J] Journal of Pediatric and Neonatal Individualized Medicine, 2020, 9(1): e090139. DOI: 10.7363/090139
doi: 10.7363/090139
[20]   SENCIO V, MACHADO M G, TROTTEIN F. The lung-gut axis during viral respiratory infections: the impact of gut dysbiosis on secondary disease outcomes[J]. Mucosal Immunology, 2021, 14(2): 296-304. DOI: 10.1038/s41385-020-00361-8
doi: 10.1038/s41385-020-00361-8
[21]   DHAR D, MOHANTY A. Gut microbiota and Covid-19-possible link and implications[J]. Virus Research, 2020, 285: 198018. DOI: 10.1016/j.virusres.2020.198018
doi: 10.1016/j.virusres.2020.198018
[22]   肖锶瑶,张纾难.肠道菌群和呼吸系统疾病相关性的研究进展[J].中国全科医学,2021,24(9):1165-1172. DOI:10.12114/j.issn.1007-9572.2021.00.003
XIAO S Y, ZHANG S N. Recent advances in the relationship between intestinal flora and respiratory diseases[J]. Chinese General Practice, 2021, 24(9): 1165-1172. (in Chinese with English abstract)
doi: 10.12114/j.issn.1007-9572.2021.00.003
[23]   HARPER A, VIJAYAKUMAR V, OUWEHAND A C, et al. Viral infections, the microbiome, and probiotics[J]. Frontiers in Cellular and Infection Microbiology, 2021, 10: 596166. DOI: 10.3389/fcimb.2020.596166
doi: 10.3389/fcimb.2020.596166
[24]   ZHANG Q, HU J, FENG J W, et al. Influenza infection elicits an expansion of gut population of endogenous Bifidobacterium animalis which protects mice against infection[J]. Genome Biology, 2020, 21(1): 99. DOI: 10.1186/s13059-020-02007-1
doi: 10.1186/s13059-020-02007-1
[25]   LEHTORANTA L, PITKÄRANTA A, KORPELA R. Probiotics in respiratory virus infections[J]. European Journal of Clinical Microbiology & Infectious Diseases, 2014, 33(8): 1289-1302. DOI: 10.1007/s10096-014-2086-y
doi: 10.1007/s10096-014-2086-y
[26]   SALMINEN S, NYBOM S, MERILUOTO J, et al. Interaction of probiotics and pathogens—benefits to human health?[J]. Current Opinion in Biotechnology, 2010, 21(2): 157-167. DOI: 10.1016/j.copbio.2010.03.016
doi: 10.1016/j.copbio.2010.03.016
[27]   WANG Z Y, CHAI W D, BURWINKEL M, et al. Inhibitory influence of Enterococcus faecium on the propagation of swine influenza A virus in vitro [J]. PLoS ONE, 2013, 8(1): e53043. DOI: 10.1371/journal.pone.0053043
doi: 10.1371/journal.pone.0053043
[28]   STAROSILA D, RYBALKO S, VARBANETZ L, et al. Anti-influenza activity of a Bacillus subtilis probiotic strain[J]. Antimicrobial Agents and Chemotherapy, 2017, 61(7): e00539-17. DOI: 10.1128/AAC.00539-17
doi: 10.1128/AAC.00539-17
[29]   MEYERHOFF R R, NIGHOT P K, ALI R A, et al. Characterization of Turkey inducible nitric oxide synthase and identification of its expression in the intestinal epithelium following astrovirus infection[J]. Comparative Immunology, Microbiology and Infectious Diseases, 2012, 35(1): 63-69. DOI: 10.1016/j.cimid.2011.10.002
doi: 10.1016/j.cimid.2011.10.002
[30]   SERKEDJIEVA J, DANOVA S, IVANOVA I. Antiinfluenza virus activity of a bacteriocin produced by Lactobacillus delbrueckii [J]. Applied Biochemistry and Biotechnology, 2000, 88: 285-298. DOI: 10.1385/ABAB:88:1-3:285
doi: 10.1385/ABAB:88:1-3:285
[31]   MELANO I, KUO L L, LO Y C, et al. Effects of basic amino acids and their derivatives on SARS-CoV-2 and influenza-A virus infection[J]. Viruses, 2021, 13(7): 1301. DOI: 10.3390/v13071301
doi: 10.3390/v13071301
[32]   LIU B Y, CHEN X L, ZHOU L, et al. The gut microbiota of bats confers tolerance to influenza virus (H1N1) infection in mice[J]. Transboundary and Emerging Diseases, 2022, 69(5): e1469-e1487. DOI: 10.1111/tbed.14478
doi: 10.1111/tbed.14478
[33]   SINGH K, RAO A. Probiotics: a potential immunomodulator in COVID-19 infection management[J]. Nutrition Research, 2021, 87: 1-12. DOI: 10.1016/j.nutres.2020.12.014
doi: 10.1016/j.nutres.2020.12.014
[34]   崔治中,崔保安.兽医免疫学[M].北京:中国农业出版社,2004:19.
CUI Z Z, CUI B A. Veterinary Immunology[M]. Beijing: China Agriculture Press, 2004: 19. (in Chinese)
[35]   ANTUSHEVICH H. Interplays between inflammasomes and viruses, bacteria (pathogenic and probiotic), yeasts and parasites[J]. Immunology Letters, 2020, 228: 1-14. DOI: 10.1016/j.imlet.2020.09.004
doi: 10.1016/j.imlet.2020.09.004
[36]   CHIBA Y, KAN S D, NAGATA S, et al. Well-controlled proinflammatory cytokine responses of Peyer’s patch cells to probiotic Lactobacillus casei [J]. Immunology, 2010, 130(3): 352-362. DOI: 10.1111/j.1365-2567.2009.03204.x
doi: 10.1111/j.1365-2567.2009.03204.x
[37]   BELKACEM N, BOURDET-SICARD R, TAHA M K. Lactobacillus paracasei feeding improves the control of secondary experimental meningococcal infection in flu-infected mice[J]. BMC Infectious Diseases, 2018, 18: 167. DOI: 10.1186/s12879-018-3086-9
doi: 10.1186/s12879-018-3086-9
[38]   YANG Y, SONG H, WANG L, et al. Antiviral effects of a probiotic metabolic products against transmissible gastroenteritis coronavirus[J]. Journal of Probiotics & Health, 2017, 5(3):184. DOI: 10.4172/2329-8901.1000184
doi: 10.4172/2329-8901.1000184
[39]   PARK M K, NGO V, KWON Y M, et al. Lactobacillus plantarum DK119 as a probiotic confers protection against influenza virus by modulating innate immunity[J]. PLoS ONE, 2013, 8(10): e75368. DOI: 10.1371/journal.pone.0075368
doi: 10.1371/journal.pone.0075368
[40]   KAWAHARA T, TAKAHASHI T, OISHI K, et al. Consecutive oral administration of Bifidobacterium longum MM-2 improves the defense system against influenza virus infection by enhancing natural killer cell activity in a murine model[J]. Microbiology and Immunology, 2015, 59(1): 1-12. DOI: 10.1111/1348-0421.12210
doi: 10.1111/1348-0421.12210
[41]   GROEGER D, SCHIAVI E, GRANT R, et al. Intranasal Bifidobacterium longum protects against viral-induced lung inflammation and injury in a murine model of lethal influenza infection[J]. EBioMedicine, 2020, 60: 102981. DOI: 10.1016/j.ebiom.2020.102981
doi: 10.1016/j.ebiom.2020.102981
[42]   ZOLNIKOVA O, KOMKOVA I, POTSKHERASHVILI N, et al. Application of probiotics for acute respiratory tract infections[J]. Italian Journal of Medicine, 2018, 12(1): 32. DOI: 10.4081/itjm.2018.931
doi: 10.4081/itjm.2018.931
[43]   OU Y C, FU H C, TSENG C W, et al. The influence of probiotics on genital high-risk human papilloma virus clearance and quality of cervical smear: a randomized placebo-controlled trial[J]. BMC Women’s Health, 2019, 19: 103. DOI: 10.1186/s12905-019-0798-y
doi: 10.1186/s12905-019-0798-y
[44]   LEE Y N, YOUN H N, KWON J H, et al. Sublingual administration of Lactobacillus rhamnosus affects respiratory immune responses and facilitates protection against influenza virus infection in mice[J]. Antiviral Research, 2013, 98(2): 284-290. DOI: 10.1016/j.antiviral.2013.03.013
doi: 10.1016/j.antiviral.2013.03.013
[45]   KIKUCHI Y, KUNITOH-ASARI A, HAYAKAWA K, et al. Oral administration of Lactobacillus plantarum strain AYA enhances IgA secretion and provides survival protection against influenza virus infection in mice[J]. PLoS ONE, 2014, 9(1): e86416. DOI: 10.1371/journal.pone.0086416
doi: 10.1371/journal.pone.0086416
[46]   ALQAZLAN N, ALIZADEH M, BOODHOO N, et al. Probiotic lactobacilli limit avian influenza virus subtype H9N2 replication in chicken cecal tonsil mononuclear cells[J]. Vaccines, 2020, 8(4): 605. DOI: 10.3390/vaccines8040605
doi: 10.3390/vaccines8040605
[47]   SEO B J, RATHER I A, KUMAR V J R, et al. Evaluation of Leuconostoc mesenteroides YML003 as a probiotic against low-pathogenic avian influenza (H9N2) virus in chickens[J]. Journal of Applied Microbiology, 2012, 113(1): 163-171. DOI: 10.1111/j.1365-2672.2012.05326.x
doi: 10.1111/j.1365-2672.2012.05326.x
[48]   HU X T, ZHAO Y, YANG Y, et al. Akkermansia muciniphila improves host defense against influenza virus infection[J]. Frontiers in Microbiology, 2021, 11: 586476. DOI: 10.3389/fmicb.2020.586476
doi: 10.3389/fmicb.2020.586476
[49]   MAHOOTI M, ABDOLALIPOUR E, SALEHZADEH A, et al. Immunomodulatory and prophylactic effects of Bifidobacterium bifidum probiotic strain on influenza infection in mice[J]. World Journal of Microbiology and Biotechnology, 2019, 35(6): 91. DOI: 10.1007/s11274-019-2667-0
doi: 10.1007/s11274-019-2667-0
[50]   KAWASHIMA T, HAYASHI K, KOSAKA A, et al. Lactobacillus plantarum strain YU from fermented foods activates Th1 and protective immune responses[J]. International Immunopharmacology, 2011, 11(12): 2017-2024. DOI: 10.1016/j.intimp.2011.08.013
doi: 10.1016/j.intimp.2011.08.013
[51]   SONG J A, KIM H J, HONG S K, et al. Oral intake of Lactobacillus rhamnosus M21 enhances the survival rate of mice lethally infected with influenza virus[J]. Journal of Microbiology, Immunology and Infection, 2016, 49(1): 16-23. DOI: 10.1016/j.jmii.2014.07.011
doi: 10.1016/j.jmii.2014.07.011
[52]   JUNG Y J, LEE Y T, LE NGO V, et al. Heat-killed Lactobacillus casei confers broad protection against influenza A virus primary infection and develops heterosubtypic immunity against future secondary infection[J]. Scientific Reports, 2017, 7: 17360. DOI: 10.1038/s41598-017-17487-8
doi: 10.1038/s41598-017-17487-8
[53]   SHOJADOOST B, KULKARNI R R, BRISBIN J T, et al. Interactions between lactobacilli and chicken macrophages induce antiviral responses against avian influenza virus[J]. Research in Veterinary Science, 2019, 125: 441-450. DOI: 10.1016/j.rvsc.2017.10.007
doi: 10.1016/j.rvsc.2017.10.007
[54]   SUN Y X, QIAN J, XU X H, et al. Dendritic cell-targeted recombinant Lactobacilli induce DC activation and elicit specific immune responses against G57 genotype of avian H9N2 influenza virus infection[J]. Veterinary Microbiology, 2018, 223: 9-20. DOI: 10.1016/j.vetmic.2018.07.009
doi: 10.1016/j.vetmic.2018.07.009
[55]   JOUNAI K, IKADO K, SUGIMURA T, et al. Spherical lactic acid bacteria activate plasmacytoid dendritic cells immunomodulatory function via TLR9-dependent crosstalk with myeloid dendritic cells[J]. PLoS ONE, 2012, 7(4): e32588. DOI: 10.1371/journal.pone.0032588
doi: 10.1371/journal.pone.0032588
[56]   KUMOVA O K, FIKE A J, THAYER J L, et al. Lung transcriptional unresponsiveness and loss of early influenza virus control in infected neonates is prevented by intranasal Lactobacillus rhamnosus GG[J]. PLoS Pathogens, 2019, 15(10): e1008072. DOI: 10.1371/journal.ppat.1008072
doi: 10.1371/journal.ppat.1008072
[57]   CHEN M F, WENG K F, HUANG S Y, et al. Pretreatment with a heat-killed probiotic modulates monocyte chemo-attractant protein-1 and reduces the pathogenicity of influenza and enterovirus 71 infections[J]. Mucosal Immunology, 2017, 10(1): 215-227. DOI: 10.1038/mi.2016.31
doi: 10.1038/mi.2016.31
[58]   SUNDARARAMAN A, RAY M, RAVINDRA P V, et al. Role of probiotics to combat viral infections with emphasis on COVID-19[J]. Applied Microbiology and Biotechnology, 2020, 104(19): 8089-8104. DOI: 10.1007/s00253-020-10832-4
doi: 10.1007/s00253-020-10832-4
[59]   YANG W T, YANG G L, WANG Q, et al. Protective efficacy of Fc targeting conserved influenza virus M2e antigen expressed by Lactobacillus plantarum [J]. Antiviral Research, 2017, 138: 9-21. DOI: 10.1016/j.antiviral.2016.11.025
doi: 10.1016/j.antiviral.2016.11.025
[60]   KASSAA I AL. New Insights on Antiviral Probiotics[M]. Cham, Switzerland: Springer Nature, 2016. DOI: 10.1007/978-3-319-49688-7
doi: 10.1007/978-3-319-49688-7
[61]   KISO M, TAKANO R, SAKABE S, et al. Protective efficacy of orally administered, heat-killed Lactobacillus pentosus b240 against influenza A virus[J]. Scientific Reports, 2013, 3: 1563. DOI: 10.1038/srep01563
doi: 10.1038/srep01563
[62]   NAKAYAMA Y, MORIYA T, SAKAI F, et al. Oral administration of Lactobacillus gasseri SBT2055 is effective for preventing influenza in mice[J]. Scientific Reports, 2014, 4: 4638. DOI: 10.1038/srep04638
doi: 10.1038/srep04638
[63]   GAO X, HUANG L L, ZHU L Q, et al. Inhibition of H9N2 virus invasion into dendritic cells by the S-layer protein from L. acidophilus ATCC 4356[J]. Frontiers in Cellular and Infection Microbiology, 2016, 6: 137. DOI: 10.3389/fcimb.2016.00137
doi: 10.3389/fcimb.2016.00137
[64]   BESSELINK M G, VAN SANTVOORT H C, BUSKENS E, et al. Probiotic prophylaxis in predicted severe acute pancreatitis: a randomised, double-blind, placebo-controlled trial[J]. The Lancet, 2008, 371(9613): 651-659. DOI: 10.1016/S0140-6736(08)60207-X
doi: 10.1016/S0140-6736(08)60207-X
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